Research Article |
Corresponding author: Hélcio R. Gil-Santana ( helciogil@hotmail.com ) Academic editor: Guanyang Zhang
© 2017 Hélcio R. Gil-Santana, Adriana Trevizoli Salomão, Jader de Oliveira.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Gil-Santana HR, Salomão AT, Oliveira J (2017) First description of the male and redescription of the female of Parahiranetis salgadoi Gil-Santana (Hemiptera, Reduviidae, Harpactorinae). ZooKeys 671: 19-48. https://doi.org/10.3897/zookeys.671.11985
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The male of Parahiranetis salgadoi Gil-Santana, 2015 is described for the first time, with a redescription of the female of this species based on additional specimens. Comments on possible mimicry and crypsis exhibited by adults and nymphs of this species, respectively, are provided.
Graptocleptes , Harpactorini , Heteroptera , Hiranetis , Neotropics, sexual dimorphism, wasp mimicry
Harpactorinae is the largest subfamily of Reduviidae and is represented by the tribes Apiomerini and Harpactorini in the Neotropical region (
Sexual dimorphism has been recorded in several species of Harpactorini. In a number of species belonging to Zelus Fabricius, 1803, for example, males and females differ drastically in size, body configuration, and coloration (
Male genitalia have been found to provide useful diagnostic characteristics for distinguishing species within the genera of Harpactorini (e.g.
Parahiranetis is a monotypic genus containing the wasp-mimicking species P. salgadoi Gil-Santana, 2015. This genus was described based on two female specimens collected in the middle of last century (holotype) and in its first half (paratype) in Rio de Janeiro, Brazil (
The specimens described here are deposited in the Entomological Collection of the National Museum of the Federal University of Rio de Janeiro (Museu Nacional da Universidade Federal do Rio de Janeiro), Rio de Janeiro, Brazil (
All fieldwork, including observation and collection of the living specimens from the state of São Paulo, was undertaken by the second author (ATS), who also pinned and dried these specimens for subsequent study. She obtained images of live specimens (Figs
Scanning electron microscopy images (Figs
The photo of the female holotype of Isthmiade braconides (Perty, 1832) (Coleoptera: Cerambycidae: Cerambycinae: Rhinotragini) (Fig.
All remaining figures were produced by the first author (HRG-S). The fixed adults, microscopic preparations and genitalia were photographed using digital cameras (Nikon D5200 with a Nikon Macro Lens 105 mm, Sony DSC-W830 and Sony DSC-HX400V). Drawings were made using a camera lucida. For clarity, the vestiture (setation) was omitted in the ink drawings of Figs
Observations were made using a stereoscope microscope (Zeiss Stemi) and a compound microscope (Leica CME). Measurements were made using a micrometer eyepiece. The total length of the head was measured excluding the neck, for better uniformity of this measurement. Antennal segments were cleared in 20% NaOH solution for 72 hours for microscopic examination (Figs
General morphological terminology mainly follows
Parahiranetis
salgadoi
Gil-Santana, 2015: 32 [description], 33 [Figures
Parahiranetis salgadoi. Type material. BRAZIL, Rio de Janeiro, Rio de Janeiro Municipality, Holotype (female): Floresta da Tijuca [Tijuca Forest] / D[istrito] Federal [currently, Rio de Janeiro] / 31.x.1951 / C. A. Campos Seabra [leg.] // [ex] Coleção [Collection] Campos Seabra // ‘XXXII’ // Holotipo [red label] // Parahiranetis salgadoi Gil-Santana, 2015 / Gil-Santana det., (
BRAZIL, São Paulo, Jundiaí, Serra do Japi, 21.x.2014, 23°13'S, 46°56'W, 1.013 m.a.s.l., 01 female, 01 male, 30.x.2014, 23°14'S, 46°55'W, 900 m.a.s.l., 01 male, 31.x.2014, 23°14'S, 46°55'W, 900 m.a.s.l., 02 males, 03.xi.2014, 23°14'S, 46°55'W, 900 m.a.s.l., 03 females, 01 male, 14.xi.2014, 23°14'S, 46°55'W, 900 m.a.s.l., 01 female, 01 male, 21.xi.2014, 23°13'S, 46°56'W, 1.013 m.a.s.l., 02 males, 1.014 m.a.s.l., 02 females, 01 male, A.T. Salomão leg., (
Male. Measurements are given in Table
Measurements (mm) of male specimens (N=9) of P. salgadoi from São Paulo State.
Measurement | Mean | SD | Maximum | Minimum |
---|---|---|---|---|
Body length to tip of hemelytra | 18.0 | 0.82 | 19.5 | 17.0 |
Body length to tip of abdomen | 13.75 | 0.53 | 14.7 | 13.2 |
Head length (excluding neck) | 2.26 | 0.04 | 2.3 | 2.2 |
Anteocular portion length | 0.93 | 0.04 | 1.0 | 0.85 |
Postocular portion length | 0.71 | 0.03 | 0.75 | 0.65 |
Head width across eyes | 1.7 | 0.05 | 1.8 | 1.62 |
Interocular distance | 0.85 | 0.06 | 0.9 | 0.71 |
Transverse width of eye | 0.39 | 0.01 | 0.4 | 0.38 |
Length of eye | 0.61 | 0.02 | 0.67 | 0.60 |
Antennal segment I length | 5.48 | 0.12 | 5.7 | 5.3 |
Antennal segment II length | 1.66 | 0.06 | 1.7 | 1.5 |
Ant. segment III length (n = 6) | 9.25 | 0.35 | 9.7 | 8.9 |
Ant. segment IV length (n = 3) | 2.03 | 0.15 | 2.2 | 1.9 |
Max. width ant. seg. III (n = 6) | 0.26 | 0.02 | 0.32 | 0.24 |
Labial segment II length | 1.33 | 0.08 | 1.5 | 1.25 |
Labial segment III length | 1.33 | 0.08 | 1.5 | 1.25 |
Labial segment IV length | 0.45 | 0.05 | 0.5 | 0.35 |
Ocellar tubercle width | 0.95 | 0.05 | 1.0 | 0.9 |
Pronotum length | 2.57 | 0.17 | 2.95 | 2.4 |
Pronotum maximum width | 2.95 | 0.14 | 3.3 | 2.85 |
Scutellum length | 0.93 | 0.03 | 1.0 | 0.9 |
Fore femur length | 5.62 | 0.07 | 5.7 | 5.6 |
Fore tibia length | 5.97 | 0.14 | 6.25 | 5.8 |
Fore tarsus length | 0.66 | 0.009 | 0.67 | 0.65 |
Mid femur length | 4.9 | 0.09 | 5.0 | 4.8 |
Mid tibia length | 6.3 | 0.17 | 6.5 | 6.0 |
Mid tarsus length | 0.66 | 0.009 | 0.67 | 0.65 |
Hind femur length | 6.7 | 0.14 | 6.9 | 6.5 |
Hind tibia length | 9.4 | 0.33 | 9.8 | 9.0 |
Hind tarsus length | 0.7 | 0.02 | 0.75 | 0.65 |
Abdomen length | 7.78 | 0.39 | 8.5 | 7.2 |
Abdomen maximum width | 2.3 | 0.36 | 2.7 | 1.8 |
Coloration: general coloration black, sometimes brownish, with reddish portions (Figs
Structure and vestiture: integument mostly shiny, smooth. In some specimens, a thin layer or small patches of sticky substance variably cover integument of antennal segment I and legs, especially on femora and tibiae of fore and mid legs, and/or are scattered on thorax and sternites. Head (Figs
Parahiranetis salgadoi Gil-Santana, male antenna. 5 apical half of segment I, segment II and basal portion of segment III 6 segment I, midportion 7–8 segment II 7 basal half 8 distal half 9–10 segment III 9 basal portion 10 small area under higher magnification (a stiff darkened seta contoured; black arrows point to thin pale setae; white arrows point to blackish stiff adpressed setae) 11 segments III (distal half) and IV (basal half). (s: point of clear separation between the thickened and thinner portions; a: articulation between segment III and IV; IV: fourth segment, partially broken) 12 segment III, region of the transition between the thickened and thinner portions 13 segment IV, distal half. Scale bars: 1.0 mm (5, 11); 0.3 mm (6–9, 12, 13); 0.1 mm (10).
Parahiranetis salgadoi Gil-Santana, male thorax. 14 pronotum, dorsal view 15 setae of the midlongitudinal line of the pronotum with flocky patches of wax-like substance A–B under progressively higher magnification 16 meso- and metathorax, ventral view. Scale bars: : 0.5 mm (14, 16); 0.05 mm (15A); 0.02 mm (15B).
Parahiranetis salgadoi Gil-Santana, male. 17 hemelytron and hind wing 18 sternites II–IV, lateral view 19 patch of whitish, minute, thin, adpressed setae on midlateral portion of sternite IV, with few amount of wax-like substance on setae 20 upper portion of the same patch of minute setae on sternite IV under higher magnification. Scale bars: 3.0 mm (17); 0.5 mm (18); 0.2 mm (19); 0.02 mm (20).
Male genitalia (Figs
Parahiranetis salgadoi Gil-Santana, male genitalia. 21 dorsal view 22 pygophore and right paramere, dorsal view 23 pygophore without parameres, lateral view 24 shape of median process of pygophore, ventral view 25 left paramere 26–27 pygophore with endosoma completely inflated, dorsal view. (ao: anterior opening; bpa: basal plate arm; db: dorsal bridge; fp: pair of elongate, flat processes; L: globe-shaped lobe in distal third of endosoma; mp: medial process of pygophore; pa: paramere). Scale bars: 0.2 mm (21); 0.5 mm (22–23); 0.3 mm (24–25); 1.0 mm (26–27).
Parahiranetis salgadoi Gil-Santana, male genitalia. 28–29 pygophore with endosoma completely inflated 28 latero-dorsal view 29 ventral view 30–32 phallus 30 lateral view 31–32 dorsal view. (ag: apicolateral group of spiny processes of the endosoma; bpa: basal plate arm; fp: pair of elongate, flat processes; L: globe-shaped lobe in distal third of endosoma; LB: large lobe, middle third of the phallothecal plate; LS: lateral large spine of the phallothecal plate; u: U-shaped basal process). Scale bar: 1.0 mm.
Parahiranetis salgadoi Gil-Santana, male genitalia, dorsal view. 33 phallus with expanded endosoma 34 articulatory apparatus 35–36 dorsal phallothecal plate and struts 35 basal portion 36 apical two-thirds. (ag: apicolateral group of spiny processes of the endosoma; bpa: basal plate arm; bpb: basal plate bridge; fp: pair of elongate, flat processes; LB: large lobe, middle third of the phallothecal plate; LS: lateral large spine of the phallothecal plate; m: median subspherical process; pd: pedicel; st: struts). Scale bars: 0.5 mm (33); 0.3 mm (34–35); 0.2 mm (36).
Parahiranetis salgadoi Gil-Santana, male genitalia, dorsal view. 37–40 endosoma portions and processes 37 globe-shaped lobe in distal third 38 distal portion 39 basal portion 40 midportion 41 a pair of elongate, flat processes. (ag: apicolateral group of spiny processes of the endosoma; fp: pair of elongate, flat processes; m: median subspherical process; u: U-shaped basal process). Scale bars: 0.3 mm (37–39); 0.2 mm (40–41).
Female. Figures
Coloration: yellowish rings on femora with the following relative values: on fore femora, the annulus is approximately 1/10 to 1/11 as long as fore femur and midpoint of annulus is about 8 to 12% distal from midpoint of fore femur; on mid femora, annulus is approximately 1/7 to 1/8 as long as mid femur and midpoint of annulus is about 8 to 10% distal from midpoint of mid femur, while on hind femora, the same relationships are about 1/7 to 1/11 and 8 to 9%, respectively. On abdominal sternites, generally reddish coloration extends to basolateral portion of sternite V (Figs
Structure: Head: approximately 1.47 to 1.65 times as long as width across eyes (length measured excluding neck) in the type specimens; labial segment II (first apparent) slightly longer than segment III; antennal segment III somewhat thicker in basal portion (Figs
Measurements (mm) of female specimens (N = 7) of P. salgadoi from São Paulo State.
Measurement | Mean | SD | Maximum | Minimum |
---|---|---|---|---|
Body length to tip of hemelytra | 22.5 | 0.64 | 23.5 | 21.5 |
Body length to tip of abdomen | 18.45 | 0.57 | 19.2 | 17.5 |
Head length (excluding neck) | 2.6 | 0.07 | 2.7 | 2.5 |
Anteocular portion length | 1.09 | 0.07 | 1.2 | 1.0 |
Postocular portion length | 0.77 | 0.07 | 0.9 | 0.7 |
Head width across eyes | 1.86 | 0.08 | 2.0 | 1.75 |
Interocular distance | 0.98 | 0.02 | 1.0 | 0.95 |
Transverse width of right eye | 0.42 | 0.04 | 0.5 | 0.38 |
Length of right eye | 0.68 | 0.03 | 0.75 | 0.65 |
Antennal segment I length | 6.6 | 0.18 | 6.9 | 6.4 |
Antennal segment II length | 2.42 | 0.21 | 2.9 | 2.3 |
Ant. segment III length (n = 4) | 8.02 | 0.25 | 8.3 | 7.7 |
Ant. segment IV length (n = 4) | 2.11 | 0.19 | 2.3 | 1.9 |
Max. width ant. seg. III (n = 6) | 0.15 | 0.01 | 0.17 | 0.14 |
Labial segment II length | 1.51 | 0.03 | 1.6 | 1.5 |
Labial segment III length | 1.59 | 0.03 | 1.65 | 1.55 |
Labial segment IV length | 0.53 | 0.04 | 0.6 | 0.45 |
Ocellar tubercle width | 1.04 | 0.07 | 1.2 | 1.0 |
Pronotum length | 3.18 | 0.15 | 3.4 | 3.0 |
Pronotum maximum width | 3.77 | 0.16 | 4.0 | 3.5 |
Scutellum length | 1.14 | 0.11 | 1.25 | 1.0 |
Fore femur length | 6.28 | 0.26 | 6.7 | 6.0 |
Fore tibia length | 6.68 | 0.1 | 6.8 | 6.5 |
Fore tarsus length | 0.75 | 0.0 | 0.75 | 0.75 |
Mid femur length | 5.48 | 0.21 | 5.9 | 5.3 |
Mid tibia length | 7.2 | 0.29 | 7.5 | 6.8 |
Mid tarsus length | 0.77 | 0.02 | 0.8 | 0.75 |
Hind femur length | 7.92 | 0.32 | 8.5 | 7.4 |
Hind tibia length | 10.8 | 0.34 | 11.5 | 10.4 |
Hind tarsus length | 0.81 | 0.03 | 0.85 | 0.75 |
Abdomen length | 11.15 | 0.58 | 12.0 | 10.5 |
Abdomen maximum width | 3.7 | 0.36 | 4.1 | 3.1 |
External genitalia (Figs
Parahiranetis salgadoi Gil-Santana, female. 46 head, fore coxae, fore trochanters and basal half of fore femora, ventral view 47–52 antenna 47 apex of segment I, segment II and basal portion of segment III 48 apex of segment I and segments II–IV. (ap: apex; b: basal portion) 49 basal portion of segment I 50 apex of segment I and basal portion of segment II 51 apex of segment II and basal portion of segment III 52 apex of segment IV. Scale bars: 0.5 mm (46–47); 2.0 mm (48); 0.3 mm (49–52).
Parahiranetis salgadoi Gil-Santana, female. 53–54 dorsal view 53 posterior half of pronotum and scutellum 54 scutellum 55–56 abdominal segments II–IV, lateral view 55 patches of whitish, minute, thin, adpressed setae on midlateral portions of sternite III–IV without wax-like substance 56 the same with large amount of wax-like substance on setae 57–58 female genitalia 57 postero-ventral view (fg: first gonapophysis; g: gonoplac; s: syntergite 9/10) 58 posterior view. Scale bars: 1.0 mm (53); 0.2 mm (54, 58); 2.0 mm (55–56); 0.5 mm (57).
In the type specimens, the head and the body length to the tip of the hemelytra are slightly longer than those in the specimens from the state of São Paulo. The body length to the tip of the abdomen is also slightly longer in the holotype (Table
Measurement | holotype | paratype | females from São Paulo State (maximum-minimum) |
---|---|---|---|
Body length to tip of hemelytra | 24.5 | 24.2 | 23.5–21.5 |
Body length to tip of abdomen | 19.5 | 19.1 | 19.2–17.5 |
Head length (excluding neck) | 3.3 | 3.1 | 2.7–2.5 |
Head width across eyes | 2.0 | 2.1 | 2.0–1.75 |
Interocular distance | 1.1 | 1.0 | 1.0–0.95 |
Abdomen length | 10.5 | 11.0 | 12–10.5 |
Abdomen maximum width | 4.2 | 4.0 | 4.1–3.1 |
Brazil, in states of Rio de Janeiro and São Paulo (Atlantic tropical moist forest and Atlantic semideciduous forest, respectively).
Both nymphs and adults were observed in aggregates on tree trunks, where most individuals remained relatively motionless (Figs
Nymphs were not collected to allow them to reach the adult stage in the wild. Consequently, it is not possible to provide a formal description of them at this time.
Examination of additional specimens, including males, allowed us to provide a more complete description of the adults of Parahiranetis salgadoi.
The sticky, viscous substance that covers the integument of some species of Harpactorini, particularly their fore and mid legs, is produced by specialized epidermal glands. These species use it to catch their prey (
Body parts covered with patches of setae with whitish wax-like material have been registered in some Harpactorini species, such as Cosmoclopius curacavensis Cobben & Wygodzinsky, 1975 (
Differences in body size and in the structure and vestiture of the third antennal segment were clear-cut enough to be considered as sexually dimorphic in P. salgadoi. Despite the small number of measurements obtained for the third antennal segments (because they were broken and lost in some specimens), adults can be sexed readily with the naked eye, by observing these two traits. Firstly, females were larger than males in almost all the morphological characteristics measured. Secondly, the third antennal segment was longer in males than in females, both in absolute and in relative terms (i.e. total length and the ratio between the third and first antennal segments, respectively). Moreover, in males, the third antennal segment was distinctly thickened, approximately in its basal two-thirds, with the thicker portion clearly separated in relation to the thinner, distal portion (Figs
Some slight differences were also noted between the type specimens and the specimens from São Paulo. These are very probably due to intraspecific variation. However, measurements of the head and the ratio of head length to maximum width across the eyes are important for separating Parahiranetis from related genera, especially Hiranetis (
1) Graptocleptes: Head elongate, approximately 1.1 to 1.3 times as long as width across eyes, sparsely setose; legs thicker; fore femur shorter than head and pronotum together and of uniform thickness.
2) Hiranetis: Head gibbous, large, approximately as long as width across eyes, densely setose on ventral and post-ocular portions; legs elongated, slender; fore femur subequally longer than head and pronotum together, thicker basally.
3) Parahiranetis: Head elongate, approximately 1.3 times to 1.7 as long as width across eyes, densely setose on ventral and post-ocular portions; legs elongated, slender; fore femur subequally longer than head and pronotum together, thicker basally.
The male genitalia of P. salgadoi showed some similarities to those of G. bicolor (
Moreover, the male genitalia of P. salgadoi differ from those of both of those species in some parts. Firstly, the basal plate arms of the articulatory apparatus are clearly longer in this species (Figs
Historically, only the pattern of yellowish or straw-colored hemelytra with a median transverse black band has received attention in regards to the supposed mimicry between Harpactorini and species of hymenopteran Ichneumonidae and Braconidae (
63 Parahiranetis salgadoi, live specimens; two male adults and fifth instar nymphs on a tree trunk; red arrows point to nymphs 64 female holotype of Isthmiade braconides (Perty, 1832) (Coleoptera: Cerambycidae: Cerambycinae: Rhinotragini), deposited in the
Although there are records of color variation in some wasp-mimicking Harpactorini, at least in the species with the pattern of darkened or blackish hemelytra with yellowish pterostigmata, there is no variation in this pattern. The yellowish pterostigmata is always present (e.g.
In contrast to the adults, nymphs of P. salgadoi were quite inconspicuous on the tree trunks where they naturally occurred (Figs
We thank the staff of the Base Ecológica da Serra do Japi for their logistic support, and Steve Lingafelter for the photo of the holotype of Isthmiade braconides presented here as Fig.